Mike Thiv 2,7 , Timothe Ü S Van Der Niet 3 , Frank Rutschmann 4
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American Journal of Botany 98(1): 76–87. 2011. O LD – NEW WORLD AND TRANS-AFRICAN DISJUNCTIONS OF THAMNOSMA (RUTACEAE): INTERCONTINENTAL LONG-DISTANCE DISPERSAL AND LOCAL DIFFERENTIATION IN THE SUCCULENT BIOME 1 Mike Thiv 2,7 , Timothe ü s van der Niet3 , Frank Rutschmann 4 , Mats Thulin 5 , Thomas Brune 6 , and Hans Peter Linder 4 2 Botany Department, State Museum of Natural History Stuttgart, Rosenstein 1, 70191 Stuttgart, Germany; 3 School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa; 4 Institute for Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland; 5 Department of Systematic Biology, Uppsala University, Norbyv ä gen 18D 75236 Uppsala, Sweden; and 6 Institute of Food Science and Biotechnology, University of Hohenheim, Garbenstrasse 25, 70593 Stuttgart, Germany • Premise of the study : The succulent biome is highly fragmented throughout the Old and New World. The resulting disjunctions on global and regional scales have been explained by various hypotheses. To evaluate these, we used Thamnosma , which is restricted to the succulent biome and has trans-Atlantic and trans-African disjunctions. Its three main distribution centers are in southern North America, southern and eastern Africa including Socotra. • Methods : We conducted parsimony, maximum likelihood, and Bayesian phylogenetic analyses based on chloroplast and nu- clear sequence data. We applied molecular clock calculations using the programs BEAST and MULTIDIVTIME and biogeo- graphic reconstructions using S-DIVA and Lagrange. • Key results : Our data indicate a weakly supported paraphyly of the New World species with respect to a palaeotropical lineage, which is further subdivided into a southern African and a Horn of Africa group. The disjunctions in Thamnosma are mostly dated to the Miocene. • Conclusions : We conclude that the Old – New World disjunction of Thamnosma is likely the result of long-distance dispersal. The Miocene closure of the arid corridor between southern and eastern Africa may have caused the split within the Old World lineage, thus making a vicariance explanation feasible. The colonization of Socotra is also due to long-distance dispersal. All recent Thamnosma species are part of the succulent biome, and the North American species may have been members of the arid Neogene Madro-Tertiary Geofl ora. Phylogenetic niche conservatism, rare long-distance dispersal, and local differentiation account for the diversity among species of Thamnosma . Key words: biogeography; disjunctions; Madro-Tertiary fl ora; molecular dating; phylogeny; Rutaceae; succulent biome; Thamnosma . Schrire et al. (2005b) accounted for the diversifi cation of le- netic niche conservatism, widely distributed clades should occupy gumes with a model that incorporated phylogenetic niche con- similar habitats in remote areas, a pattern neatly demonstrated servatism with local differentiation. The tendency of lineages to in the legumes ( Lavin et al., 2004 ; Schrire et al., 2005b ). The retain their ancestral ecological niche rather than adapting to succulent biome, which is characterized by a climate with a new environments (phylogenetic niche conservatism) has has long dry season, is found in relatively small fragments and been demonstrated in diverse clades and regions ( Wiens, 2004 ; isolated regions in both South and North America, in a large Donoghue, 2008 ; Crisp et al., 2009 ). On the basis of phyloge- region in SW Africa, and from Tanzania to Pakistan. The pre- dominant growth forms in these climates are usually evergreen, sclerophyllous, nonfi re-adapted shrubs and succulents ( Mooney 1 Manuscript received 6 September 2010; revision accepted 23 November 2010. and Dunn, 1970 ; Schrire et al., 2005a ). This succulent biome The authors would like to thank Jon Rebman (SDSU, USA) and Michael has been the object of some studies (e.g., Lavin et al., 2004 ; Denslow (Rancho Santa Ana Botanic Garden, USA) for providing plant Schrire et al., 2005a , b , 2009 ). Its characteristic climate and material, Joachim Kadereit (Mainz, Germany) for helpful comments on the highly fragmented distribution make it an excellent system in manuscript, and Mohamed Ali Hubaishan (AREA Research Station which to investigate the effects of niche conservatism. Mukalla), Ahmed Said Sulaiman (EPA Socotra), Said Masood Awad The succulent biome shows a disjunction between the New Al-Gareiri (Dept. Agriculture Socotra), and Mohamed El-Mashjary (EPA and the Old World. This pattern is matched by the distribution Sanaa, all Yemen) for support of the fi eldwork in Socotra. The fi eldwork of legumes where, e.g., the genera Arcoa Urb., Diphysa Jaqu., was conducted as part of the BIOTA Yemen Project funded by the German Pictetia DC., and Chapmannia Torr. & Gray occur in North and Ministry for Research and Education (BMBF). The work was supported by grants of the German Research Foundation (DFG, Th830/1-1) and the Mesoamerica and Tetrapterocarpon Humbert, Zygocarpum Claraz-Schenkung (Switzerland) to M.T. Thulin & Lavin, Ormocarpopsis R.Vig., Ormocarpum P. Beauv., 7 Author for correspondence (e-mail: [email protected]) and Chapmannia occur in Africa. In most of these cases, the New World group fi nds its corresponding sister clade in Africa. doi:10.3732/ajb.1000339 Several hypotheses were assumed to explain this pattern. Inferring American Journal of Botany 98(1): 76–87, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 76 January 2011] Thiv et al. — THAMNOSMA 77 from physiognomical similarities, links have been proposed where three species occur in the southern continent from An- between succulent biome taxa and dry boreotropical and gola to the northern regions of South Africa, and another three Madrean-Tethyan representatives ( Lavin et al., 2000 ). Based species grow around the Horn of Africa extending to southern on palaeontological and geological evidence, Tiffney (1985b) Arabia and the island of Socotra ( Thulin, 1999 ) ( Table 1 , Fig. 1 ). proposed an Eocene North Atlantic Land bridge (55.8 – 33.9 This pattern with trans-Atlantic and trans-African disjunctions million years ago [Ma]) linking the continents of the Northern of the succulent biome makes Thamnosma a suitable case study Hemisphere, resulting in a circumboreal, deciduous, and ever- (1) to test the hypotheses on the origin of Old and New World green heterogenous fl ora (boreotropical hypothesis, Wolfe, disjunctions in the succulent biome, (2) to investigate the “ arid 1975 ). Lavin et al. (2000) suggested that vicariance between corridor ” between southern Africa and the Horn of Africa North/Mesoamerica and Africa was possible via this land bridge region, and (3) to evaluate a vicariance origin for the Socotran for legumes. Similarily, only younger in time, the Madrean- taxon. Tethyan hypothesis suggested a common occurrence of recent and fossil sclerophyllous taxa in both southwestern North America and the Old World by the late Eocene to the late Paleo- MATERIALS AND METHODS gene (37.2 – 23 Ma, Axelrod, 1972 , 1973 , 1975 ). Another pos- sible vicariant origin of this disjunction may have been caused Taxon sampling— To resolve the interspecifi c phylogenetic relationships by an early Miocene (23 – 16 Ma) migration route via the Bering of Thamnosma , we included all 11 species of Thamnosma ( Johnston, 1983 ; land bridge, as suggested by Stebbins and Day (1967) and Tiff- Thulin, 1999 ) in a combined analysis of the ITS, matK , and the atpB-rbcL spacer ( Table 2 ), rooted with the the closely related Ruta L. ( Salvo et al., ney (1985a) . In contrast to these vicariance scenarios, the inter- 2008 ). On the basis of three chloroplast markers, Thamnosma is closely related continental disjunction of legumes in the succulent biome was to the eastern Asian, monotypic Boenninghausenia Reichb. ex Meissner, Ruta recently interpreted as result of long distance because the ages L., Haplophyllum A. Juss., and Cneoridium dumosum Hook. f. ( Salvo et al., of these lineages are much younger than the assumed vicariance 2008 ). Of those, only Cneoridium Hook. f. and Ruta could be included in our events ( Lavin et al., 2004 ). study due to availability of material. Salvo et al. (2008) found a sister-group The succulent biome is also disjunct on the African conti- relationship between Thamnosma and Boenninghausenia . Still, the monotypic Psilopeganum Hemsl. ex Forb. & Hemsl., restricted to a small area of central nent. Numerous plants (e.g., Aizoon L. [Aizoaceae], Trichoneura China ( Song et al., 2004 ), may also be closely related to Thamnosma , because Anderss. [Poaceae]) and animals (e.g., ostriches) occupy an these are the only bicarpellate genera in the Rutinae and share capitate stigmas “ arid corridor ” between southwestern and northeastern Africa and similar fl ower merosity and seed shapes (Engler, 1897, 1931 ; Salvo et al., ( Balinsky, 1962 ; Verdcourt, 1969 ; de Winter, 1971 ; J ü rgens, 2008 ). This relationship is also supported by phytochemical data (acridones of 1997 ), with an extension to Mauretania (NW Africa). The clo- type H1; da Silva et al., 1988 ). Because Psilopeganum shares more morpho- sure and widening of this arid track has been linked to Miocene logical synapomorphies with Thamnosma rather than with Boenninghausenia (cf. Salvo et al., 2008 ), it seems more likely that Thamnosma and Psilopega- uplift and rifting in Central Africa and climate changes in the num are phylogenetic sisters. However, it is unlikely that Psilopeganum